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    Differential effects of low and high temperature stress on pollen germination and tube length of mango (Mangifera indica L.) genotypes

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    Complex multiple introductions drive fall armyworm invasions into Asia and Australia

    Strain assessmentWe did not detect any C-strain individual following analysis of 138 fully assembled mitochondrial DNA genomes (mitogenomes) from Australian samples. Our results, particularly that from Northern Territory, are not dissimilar to the finding of Piggott et al.56 who detected only two (i.e., 4.2%) C-strain mtCOI haplotype individuals from a much larger (i.e., n = 48) Northern Territory sample size. Proportions of C-strain to R-strain also varied significantly across the different SEA populations (Table S1) in contrast to the patterns observed in China, India, and African nations (e.g.,22,33,34,39,57). All Australian populations analysed for their corn or rice mitochondrial haplotypes via mitogenome assemblies of whole genome sequencing data therefore contrasted with the invasive populations from SEA where in some countries (e.g., Myanmar, Vietnam) FAW with the C-strain mtCOI haplotypes made up approximately 50% of the populations examined (see Table S1 for C- and R-strains mitogenome proportions, see also Fig. 1 ‘C-strain’ and ‘R-strain’ Maximum Likelihood cladograms).Figure 1Maximum Likelihood cladograms of unique Spodoptera frugiperda C-strain and R-strain partial mitochondrial genomes based on concatenation of the 13 PCGs (11,393 bp) using IQ-Tree with 1000 UFBoot replications. Individuals in clades I, II, III, and IV (C-strain) and in Clades I, II, V (R-strain) that are in the same colour scheme (i.e., green, orange, blue, or pinks) shared 100% nucleotide identity. Mitogenome haplotypes from native individuals for both C- and R-strains are in khaki green colour. Red and dark grey dots at branch nodes represent bootstrap values of 87–100% and 74–86%, respectively. Bootstrap values  Hetexp; see60) could likewise indicate recent mixing of distinct populations from SEA that suggest multiple introductions (e.g.,33,39 cf.46,47,61,62; i.e., due to a recent bottleneck from a recent western Africa founder event).Table 1 Population genetic differentiation via pairwise FST estimates between Spodoptera frugiperda populations from the invasive ranges of Africa (Uganda, Malawi, Benin), South Asia (India), East Asia (China (Cangyuan (CY), Xinping (XP), YuanJiang (YJ)), South Korea), Southeast Asia (Malaysia (Johor, Kedah, Penang States), Laos, Vietnam, Myanmar), and Pacific/Australia (Papua New Guinea (PNG), Australia—Kununurra (Western Australia, WA), Northern Territory (NT), Strathmore, Walkamin, Burdekin, Mackay (Queensland, Qld), Wee Waa (New South Wales, NSW).Full size tableThe observed heterozygosity excess detected in all invasive range populations could be further explained as due to population sub-structure and isolation breaking through periodic migration. Significant numbers of loci (ca. 30%) were also shown to not be in Hardy–Weinberg equilibrium (HWE) especially for the Malaysian (i.e., Kedah), but also Australian (i.e., Wee Waa, NT, Kununurra), Chinese (e.g., XP), South Korean, and Malawian populations. Taken as a whole, genetic diversity results from this study therefore suggested that the invasive Asian (i.e., SA, SEA, EA) FAW populations exhibited signatures of recent mixing of previously separated populations. Simulated patterns of moth migration of various invasive FAW populations such as between Myanmar and China (e.g.,41,42,55) and to Australia54 are incompatible with the population genomic data, which suggests these were likely discrete and non-panmictic FAW populations with the most probable explanation being due to multiple origins of founding populations.Genetic differentiation analysisEstimates of pairwise genetic differentiation (FST) between populations varied significantly (Table 1) and extended to between populations within a country (e.g., Mackay vs. rest of Australia; Kedah vs. rest of Malaysia). Of interest are the pairwise estimates between different Australian FAW populations from Kununurra (Western Australia), Northern Territory, Queensland (Strathmore, Walkamin, Burdekin, Mackay) and New South Wales (Wee Waa) that represented the most recently reported invasive populations in this study, and predominantly showed significant differentiation amongst themselves (with the exception of the two Queensland populations of Mackay and partially for Walkamin) and with other SEA/SA/EA countries. The majority of non-significant population genetic differentiation estimates were in SEA where the presence of FAW was reported earlier, i.e., since 2018 (e.g.,63,64 or as early as 200865,66; see also33), while across Asia (e.g., China) since 2016 but also potentially pre-2014 (16,67; see also33).Interestingly, significant genetic differentiation was observed between populations from Yunnan province in China and populations from Myanmar, Laos, and Vietnam. Penang and Johor (Malaysia) populations were not significantly differentiated from other SE Asian populations, nor with Ugandan and Malawian populations from east Africa. Individuals from Benin and Mackay (Queensland, Australia) showed non-significant genetic differentiation with all populations except with Kedah, and for Mackay also surprisingly with the Wee Waa population from New South Wales. The South Korean population exhibited significant genetic differentiation with SE Asian population except with Mackay, India and the Yuanjiang (YJ) population in Yunnan Province. Finally, the Kedah population, being one of the earliest collected samples from Malaysia and having been maintained as a laboratory population, showed strong differentiation with all populations (and lowest nucleotide diversity, π = 0.237; Table 2) further supporting unique, non-African, introduction events in SEA. Strong genetic differentiation suggested there was limited gene flow to breakdown sub-structure between populations, and the FST estimates from these invasive populations therefore failed to support a west-to-east spread pathway for the FAW. This observation instead suggested the widespread presence of genetically distinct FAW populations, likely due to independent introductions and therefore also highlighting likely biosecurity weaknesses especially in East Asia (e.g., China, South Korea) and SEA (e.g., Malaysia).Table 2 Population statistics for Spodoptera frugiperda populations from Southeast Asia (i.e., Malaysia (MYS; Johor, Kedah, Penang), Laos, Vietnam, Myanmar), East Asia (i.e., South Korea), and Pacific/Australia (i.e., Papua New Guinea (PNG), Australia).Full size tableThe genetic diversity of Australian populations identified surprisingly complex sub-structure patterns given the short time frame of population detections across different northern Australian regions. Significant genetic differentiation between, e.g., Kununurra (WA), Northern Territory (NT), Queensland (e.g., Strathmore, Burdekin), and Wee Waa (NSW) populations suggests these populations likely derived from separate establishment events. The WA Kununurra population was not significantly differentiated from the Johor State (Malaysia), India and the Cangyuan (CY) China populations, suggesting a potential south-eastern route from SA/SEA into north-western Australia. Contrasting this, Walkamin and Mackay populations showed non-significant genetic differentiation with the Madang (PNG) population, suggesting a potential second pathway for SEA individuals to arrive at the north-eastern region of Australia. Significant genetic differentiation between WA, NT, and Qld populations suggested that at least during the early stage of pest establishment in northern Australia, there was limited gene flow to homogenise the unique genetic background carried by these distinct individuals, some of which exhibited also distinct insecticide resistance profiles48,49.PCAWe selected specific populations to compare using Principal Component Analysis (PCA) as examples to support evidence of independent introductions, as seen from Fig. 3a between China (CY, YJ, XP) populations vs. Myanmar, in Fig. 3b (within Malaysian populations between those collected from Penang and Johor States vs. Kedah State), in Fig. 3c for between China and East Africa (e.g., Uganda, Malawi), and where Benin and India individuals that grouped with either China or east Africa; and in Fig. 3d between China, Malaysia (Kedah State), and Australia (NT, NSW)). Genetic variability between Australian populations (e.g., Strathmore (QLD) vs. NT and NSW) was also evident (Fig. 3d).Figure 3Principal component analysis (PCA) showing variability between selected FAW populations from their invasive ranges. (a) China and Myanmar; (b) Kedah and Johor/Penang populations from Malaysia, (c) China and east African (Uganda/Malawi) populations, (d) Australia (Strathmore, Qld/Northern Territory + New South Wales), China, and Malaysia (Kedah) populations, (e) Australia (Strathmore, Qld) and PNG (Madang Province) populations, (f) Lao PDR/Vietnam and South Korea populations, (g) China and SE Asian (Lao PDR/Vietnam/Myanmar/Philippines/Malaysia) and Pacific/Australia (PNG) populations, and (h) Australia, China and Malaysia (Kedah) populations. Note the overall population genomic variability between countries (e.g., a, c–g) and within countries (e.g., Malaysia (b), Australia (d)). Populations with similar genomic variability are also evident, e.g., for Strathmore (e) and South Korea (f); and for Madang (e) and Lao PDR/Vietnam (f), further supporting potential different population origins of various FAW populations across the current invasive regions. The Southeast Asian and Chinese populations are overall different (g), Australia’s FAW populations showed similarity with both Southeast Asia and China (g, h).Full size imagePCA also showed that differences existed between FAW populations from the Madang Province in PNG and with the Strathmore population from Qld (Fig. 3e). The SEA FAW populations from Lao PDR/Vietnam also exhibited diversity from the South Korean population (Fig. 3f), with the South Korean and Strathmore populations largely exhibiting similar diversity patterns, while the Madang population shared similarity with Laos and Vietnam populations. Plotting all SEA populations against China clearly showed that populations from SEA were distinct from the Chinese FAW populations (Fig. 3g), while in Australia, individuals from various populations shared similarity with both Chinese and SEA FAW. Despite the connectedness of the landscape between SEA and China, SEA largely appeared to have their own FAW populations, with FAW in SEA and in China differing in their genome compositions overall as shown via PCA.PCA further enabled visualisation of genetic diversity amongst Australia FAW populations, suggesting that arrival and establishment of FAW likely involved separate introduction events that followed closely after each other and over a short timeframe. While it had been anticipated that the southward spread of FAW from SEA would necessarily lead to Australia FAW and PNG FAW to share similar genetic backgrounds, the Madang Province FAW population appeared to be different from the Strathmore (Qld) population, with the Madang population being more similar to Lao PDR/Vietnam populations, and the Strathmore population more similar to FAW from South Korea.DivMigrate analysisDirectionality of gene flow between African, South Asia (Indian), East Asia (China) and SE Asian populations were predominantly from China to east African and SE Asian populations (e.g., Figs. 4a, b, S-1; see also Table 3), while movements of FAW in Laos and Vietnam (i.e., the Indochina region) were predominantly with other SEA countries (e.g., with Myanmar and East Africa; Figs. 4c, d, S-2; see also Table 3) but with no directional movements to the three Yunnan populations (CY, XP, YJ). Migration directionality with other SE Asian populations (e.g., Johor (JB; Fig. S-3) and Penang (PN, Fig. S-4)) showed that these two populations (but especially the Johor population) were predominantly source populations for Uganda, Malawi, Philippines, Vietnam, and PNG (Fig. S-3). Bidirectional migration between Myanmar and Laos PDR populations were also detected with the Johor population from Malaysia (Fig. S-3). When India was selected as the source population, bidirectional migration events were detected with Myanmar and with the Cangyuan (CY) populations (Fig. S-5) while unidirectional migration events from India to Uganda and Malawi and to Laos were detected, and the China Yuanjian (YJ) population showed unidirectional migration to India. Unidirectional migration events from CY and YJ populations to the PNG Madang population were detected, while bidirectional migration events between PNG and Myanmar, Laos PDR, Philippines, Vietnam, and with Uganda and Malawi were also detected (Fig. S-6). No migration events were detected between the West African Benin population and with the South Korean population.Figure 4Source populations are CY (a) and XP (b). (c, d) DivMigrate analyses with edge weight setting at 0.453 showing unidirectional (yellow arrow lines) and bidirectional (blue arrow lines) migration between countries in Africa and South Asia/East Asia/SE Asia. Migration rates between populations are as provided in Table 3. (c) Vietnam (VNM) as the source population identified an incidence of unidirectional migration from Malaysia (MYS) Johor state (JB) to Vietnam, while bidirectional migration events were detected from Vietnam to other SE Asian (e.g., Philippines (PHL), Lao PDR (Lao), Myanmar (MMR)), to Pacific/Australia (i.e., Papua New Guinea (PNG)), as well as to east Africa (Uganda (UGA), Malawi (MWI)). (d) Lao PDR (LAO) as source population identified bidirectional migration events between various SEA populations and east African populations, while unidirectional migration events were identified from India (IND) and China (CHN) Yunnan populations (CY, YJ) to Laos PDR. No migration events were evident from SE Asian populations to China.(a, b) DivMigrate analyses with edge weight setting at 0.453 showing unidirectional (yellow arrow lines) and bidirectional (blue arrow lines) gene flow between countries in Africa and South Asia/East Asia/SE Asia. Significant migration rates (at alpha = 0.5) are in red and as provided in Table 3. Incidences of unidirectional migration were predominantly detected from China (CHN) Yunnan populations (CY, XP) to SE Asian populations (e.g., Myanmar (MMR), Laos PDR (Lao), Philippines (PHL)) and to east African populations (e.g., Uganda (UGA), Malawi (MWI)) (a, b).Full size imageTable 3 DivMigrate matrix showing effective migration rates calculated using GST from source to target invasive populations.Full size tableAdmixture analysisAdmixture analyses involving all Australian, Southeast Asian and South Korean populations from this study; and native populations from the Americas and Caribbean Islands, and invasive populations from Africa (Benin, Uganda, Malawi), India, and China33, provided an overall complex picture of population structure that reflected the species’ likely introduction histories across its invasive ranges.Admixture analysis that excluded New World, African and Indian populations identified four genetic clusters (i.e., K = 4) to best describe these invasive populations from SEA, and EA (i.e., China, South Korea), and Pacific/Australia (Fig. 5a). At K = 4, Australian populations from NT and NSW, YJ population from China, South Korean, and Malaysia’s Kedah population, each showed unique admixture patterns (i.e., some individuals from NT and NSW populations lacked cluster 3; most of YJ (but also some CY and XP) individuals lacked clusters 1 and 2; South Korean (e.g., MF individuals) lacked cluster 2; Malaysia’s Kedah population lacked evidence of admixture (i.e., reflecting its laboratory culture history) and was made up predominantly by individuals that belonged to cluster 4. Populations from China also differed from most populations from SEA due to the overall absence of genetic cluster 4. Taken as a whole, establishment of the FAW populations in China, Malaysia, vs. other SE Asian populations, and between Australian populations (e.g., NT/NSW cf. WA/Qld), likely involved individuals from diverse genetic background (i.e., multiple introductions). At K = 4, the majority of Australian populations appeared to contain genetic clusters similar to China (i.e., cluster 3) and to SEA (i.e., cluster 2).Figure 5Admixture and corresponding CV plots for FAW populations from: (a) Australia, China, South Korea, Lao PDR, Myanmar, Malaysia, Philippines, PNG, and Vietnam, and (b) Benin, China, India, South Korea, Lao PDR, Myanmar, Malaysia, Philippines, PNG, Tanzania, and Vietnam. Optimal ancestral genetic clusters are K = 4 for both admixture plots. Boxed individuals have unique admixture patterns at K = 4 when compared with other populations. China FAW lacked Cluster 2 (navy blue colour; present in almost all SEA and Australian FAW), while in NSW and NT some individuals lacked cluster 3. South Korea ‘MF’ population generally lacked cluster 2, while Kedah (Malaysia) showed distinct (cluster 4) pattern for all individuals. The overall same observations are evident in the admixture plot in (b), with African FAW generally exhibiting admixture patterns similar to SEA populations than to Chinese FAW. With the exception of Kedah (Malaysia) and some Chinese FAW individuals, all FAW in the invasive range showed evidence of genomic admixture (i.e., hybrid signature). The figures were generated using the POPHELPER program  and further manipulated in Microsoft PowerPoint for Mac v16.54.Full size imageOverall admixture patterns at best K = 4 in China and SEA remained unchanged when analysed together with African and Indian individuals (Fig. 5b; excluded Australia). Benin individuals were either similar to China or to SEA, while eastern African populations (e.g., Uganda, Malawi) were similar to Southeast Asian populations from e.g., Vietnam, Laos, and is in agreement with the phylogenetic inference (Fig. 3) that identified these African individuals as having loci that were derived from Southeast Asian populations.Genome-wide SNP loci demonstrated that invasive FAW populations from SEA and Australia exhibited admixed genomic signatures similar to that observed in other invasive populations33,34. While the current invasive populations in Africa and Asia likely arrived already as hybrids as suggested by Yainna et al.68, the Malaysia Kedah State population was potentially established by offspring of a non-admixed female. Distinct admixture patterns in Malaysian FAW populations between Kedah and Johor/Penang states therefore suggested that establishment of these populations was likely as separate introduction events. As reported also in Tay et al.33, the Chinese YJ population appeared to have admixed signature that differed from XP and CY populations, and suggested that the YJ population could have a different introduction history than the XP and CY populations. Similar multiple genetic signatures based on lesser nuclear markers by Jiang et al.39 also supported likely multiple introductions of China Yunnan populations. More

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    Altered gut microbiota in individuals with episodic and chronic migraine

    ParticipantsIn total, 80, 63, and 56 participants in the EM, CM, and control groups, respectively, initially agreed to participate in this study. Nevertheless, 28, 12, and 13 individuals in the EM, CM, and control groups, respectively, withdrew their participation and did not bring any fecal samples to the study site. After providing fecal samples, 10 and 6 individuals with EM and CM, respectively, reported intake of probiotics and were excluded from the analysis. No participant in the control group consumed probiotics during the study period. Eventually, 42, 45, and 43 participants in the EM, CM, and control groups, respectively, were enrolled (Fig. 1). The demographic and clinical characteristics of participants are summarized in Table 1. All participants with EM and CM used acute treatments for migraine. Moreover, 25 (59.5%) and 27 (60.0%) participants with EM and CM, respectively, received prophylactic treatment for migraine. Of the 42 participants with EM, 20 used anti-epileptic medications, 11 used beta blockers, 2 used an anti-depressant, and 1 used a calcium-channel blocker for prophylactic treatment. Of the 45 participants with CM, 23 used anti-epileptic medications, 8 used beta blockers, 1 used an anti-depressant, and no participant used calcium-channel blockers for prophylactic treatment. No participant in the EM, CM, and control groups was infected with SARS-CoV-2 before or during participation in the study.Figure 1Flow of participants in a study on the composition of gut microbiota in participants with episodic or chronic migraine.Full size imageTable 1 Demographic and clinical characteristics of participants with episodic and chronic migraine and the control.Full size tableCollection of 16 s RNA sequencing dataWe obtained 7,802,425 read sequences, accounting for 99.8% of the valid sequences from the fecal samples of 130 participants. According to barcode and primer sequence filtering, an average of 59,305 (range, 3716–90,832) observed sequences per sample was recovered for downstream analysis. Thus, 2,242,325 sequences were obtained from the controls for phylogenetic analysis, whereas 2,747,952 and 2,812,148 sequences were obtained from the EM and CM groups, respectively.Microbial diversityAlpha diversity was defined as microbial community richness and evenness. Alpha diversities in the genus richness, as evaluated by Chao1 (Fig. 2A), Shannon (Fig. 2B), and Simpson (Fig. 2C) indices, did not differ significantly among the EM, CM, and control groups. Beta diversity represented the community composition dissimilarity between samples. PCoA with the weighted UniFrac distance (Fig. 3A and Supplementary Fig. S1A, p = 0.176, permutational multivariate analysis of variance [PERMANOVA]), the unweighted UniFrac distance (Fig. 3B and Supplementary Fig. S1B, p = 0.132, PERMANOVA), and the Bray–Curtis dissimilarity index (Fig. 3C and Supplementary Fig. S1C, p = 0.220, PERMANOVA) for beta diversity at the genus level among the EM, CM, and control groups revealed that these three groups could not be separated.Figure 2Alpha diversity at the genus level using Chao1 (A), Shannon (B), and Simpson (C) indices*,†. *Controls (green) and participants with episodic migraine (blue) and chronic migraine (yellow). †In the box plots, the lower boundary of the box indicates the 25th percentile; a blue line within the box marks the median, and the upper boundary of the box indicates the 75th percentile. Whiskers above (red) and below the box (green) indicate the highest and the lowest values, respectively.Full size imageFigure 3Beta diversity of microbiota in principal coordinate analysis plot with the weighted UniFrac distance (A), the unweighted UniFrac distance (B) and the Bray–Curtis dissimilarity index (C)*. *Controls (green) and participants with episodic migraine (blue) and chronic migraine (yellow).Full size imageRelative abundance of fecal microbes between participants with EM and the controlRelative abundance of fecal microbes at the phylum level did not differ significantly among participants in the control, EM, and CM groups (Supplementary Fig. S2). Moreover, Tissierellales (p = 0.001) and Tissierellia (p = 0.001) were more abundant in the EM group than that in the control group at the order and class levels, respectively (Fig. 4A). At the family level, Peptoniphilaceae (p = 0.001) and Eubacteriaceae (p = 0.045) occurred at a significantly higher proportion in the EM group than that in the control group. Furthermore, at the genus level, the abundance of 11 genera differed significantly between the two groups, including one more abundant and 10 less abundant genera in the EM group. Catenibacterium (p = 0.031) and Olsenella (p = 0.038) had the highest relative abundance in the control and EM groups, respectively.Figure 4Taxonomic differences in fecal microbiota among participants. The fold change (log2) denotes the difference in relative abundance between participants with episodic migraine and the control (A), between those with chronic migraine and the control (B), and between those with episodic and chronic migraine (C). CM chronic migraine; EM episodic migraine.Full size imageRelative abundance of fecal microbes between participants with CM and the controlThe analysis results at the class, order, family, genus, and species levels between CM and control groups are illustrated in Fig. 4B. Tissierellia (p = 0.001), Tissierellales (p = 0.001), and Peptoniphilaceae (p = 0.001) were more abundant in the CM group than that in the control group at the class, order, and family levels, respectively; however, at the genus level, the abundances of 18 genera differed significantly, including four more abundant and 14 less abundant genera in the CM group than in the control group.Relative abundance of fecal microbes between participants with EM and CMThe analysis results at the class, order, family, and genus levels between CM and EM groups are summarized in Fig. 4C. At the class level, Bacilli (p = 0.033) were less abundant in the CM group than that in the EM group; however, at the order level, Selenomonadales (p = 0.016) and Lactobacillales (p = 0.034) were less abundant in the CM group than that in the EM group. Moreover, at the class level, Selenomonadaceae (p = 0.016) and Prevotellaceae (p = 0.012) were less abundant in the CM group than that in the EM group. Furthermore, at the genus level, PAC001212_g (p = 0.019) revealed relative positive predominancy in the CM groups, whereas Prevotella (p = 0.019), Holdemanella (p = 0.009), Olsenella (p = 0.033), Adlercreutzia (p = 0.018), and Coprococcus (p = 0.040) revealed relative positive predominancy in the EM group.Association among fecal microbiota and clinical characteristics and comorbidities of migraineAmong the five genera (Roseburia, Eubacterium_g4, Agathobacter, PAC000195_g, and Catenibacterium) depicting predominance or less-predominance both in EM and CM groups, we conducted additional analyses for clinical characteristics and migraine comorbidities.Combining the results of the 42 and 45 participants with EM and CM, respectively, the Poisson regression analysis for relative abundance of microbiota revealed that a higher composition of PAC000195_g (p = 0.040) was significantly associated with lower headache frequency (Table 2). Furthermore, Agathobacter (p = 0.009) had a negative association with severe headache intensity (Table 3). Anxiety was associated with Catenibacterium (p = 0.027); however, depression did not reveal any association with the five genera (Table 3).Table 2 The association between headache frequency and the relative abundance of microbiota.*Full size tableTable 3 The association of severe headache intensity and comorbidities with the relative abundance of microbiota*.Full size tableRelative abundance of fecal microbes in participants with EM based on prophylactic treatmentAlpha and beta diversities in participants with EM did not differ significantly based on their prophylactic treatment (Supplementary Figs S3A–C, S4A–C, and S5A–C). At the genus level, Klebsiella (p = 0.009), Enterobacteriaceae_g (p = 0.006), and Faecalibacterium (p = 0.046) were more abundant in the prophylactic group than the non-prophylactic group (Supplementary Fig. S6A).Relative abundance of fecal microbes in participants with CM based on prophylactic treatmentAlpha and beta diversities in participants with CM did not differ significantly based on prophylactic treatment (Supplementary Figs S7A–C, S8A–C, and S9A–C). Emergencia (p = 0.043), Ruthenibacterium (p = 0.005), Eggerthella (p = 0.003), PAC000743_g (p = 0.034), and Anaerostipes (p = 0.039) were more abundant in the prophylactic group, whereas PAC000196_g (p = 0.049), Fusicatenibacter (p = 0.028), and Faecalibacterium (p = 0.021) were more abundant in the non-prophylactic group at the genus level (Supplementary Fig. S6B). More

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    Warmth shifts symbionts

    Abigail Meyer from the University of Minnesota, USA, and colleagues from the USA, investigated the physiological and morphological responses to experimental warming and CO2 additions in the widespread forest lichen Evernia mesomorpha. While impacts of CO2 were largely negligible, warming and associated drying was linked to decreases in biomass, carbon assimilation and respiration rates. As well as bleaching of the lichen, indicative of death of the photobiont, the authors found evidence of shifts in internal algal communities, including increased proportions of certain algal clades under warming. While the study reveals the sensitivity of lichen algae to warming, further work is needed to reveal whether photobiont turnover may assist in lichen acclimation and recovery. More

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    Enhanced regional connectivity between western North American national parks will increase persistence of mammal species diversity

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    Migration direction in a songbird explained by two loci

    Ethics statementAnimals’ care was in accordance with institutional guidelines. Ethical permit was issued by Malmö-Lund djurförsöksetiska nämnd 5.8.18-00848/2018.Field workWe carried out the field work in Sweden during four breeding seasons (2018–2021). Adult male willow warblers were captured in their breeding territories using mist nets and playback of a song. From each bird, we collected the innermost primary feather from the right wing. From the birds that returned with a logger we also collected ~20 μl of blood from the brachial wing vein. The blood was stored in SET buffer (0.015 M NaCl, 0.05 M Tris, 0.001 M of EDTA, pH 8.0) at room temperature until deposited for permanent storage at −20 °C. We deployed Migrate Technology Ltd geolocators (Intigeo-W30Z11-DIP 12 × 5 × 4 mm, 0.32 g) and used a nylon string to mount them on birds with the “leg-loop” harness method as outlined in our previous work24. The mass of the logger relative to that of the bird was on average 3.3% (range 2.7–3.8%).The tagged birds were ringed with a numbered aluminum ring, and two, colored plastic rings for later identification in the field. In total, we tagged 466 males (349 in 2018 and 117 in 2020) at breeding territories. During the first tagging season (2018), birds were trapped at 17 locations (average 22 birds per site; range 7–30) distributed across Sweden (Fig. S1). Three of the sites were in southern Sweden to document migration routes of allopatric trochilus and three sites were located above the Arctic circle to record migratory routes of allopatric acredula, whereas the remaining (239) loggers were spread over 11 sites located in the migratory divide. Given the observed densities and distribution of hybrids after analyzing returning birds in 2019, we deployed 117 more loggers at one single site (63.439°N, 14.831°E) in 2020. We successfully retrieved tracks from 57 birds tagged in 2019 and 16 from birds tagged in 2021. In search for birds with loggers, we checked circa 3000 willow warbler males and covered an area of at least 0.5 km radius around each site the year after tagging.Geolocator data treatmentThe R package GeoLight (version 2.0)25 was used to extract and analyze locations from raw geolocator data. All twilight events were obtained with light threshold of 3 lux. The most extreme outliers were trimmed with “loessFilter” function and a K value of 3. We used GeoLight’s function “getElevation” for estimating the sun elevation angle for the breeding period: these sets of locations were used to infer the positions for autumn departure direction. In addition, we carried out a “Hill-Ekström” calibration for the longest stationary winter site during the period before the spring equinox. Winter calibration produced location sets that better reflected the winter coordinates of the main winter site in sub-Saharan Africa26. We reduced some of the inherent geolocation “noise” by applying cantered 5-day rolling means to the coordinates. The equinox periods were visually identified by inspecting standard deviations in latitude. Latitudes from equinox periods were omitted (on average autumn equinox obscured data for 45 days (range 25–68). For the main winter site, we used the longest period at which bird stayed stationary and from which in all cases begun the spring migration (mean = 118, SD = 23 days). Timing of autumn departure was estimated by manual inspection of longitudes and latitudes plotted in time series. To estimate at which longitude the birds crossed the Mediterranean, we extracted the longitude when birds crossed latitude 35 N° (Mediterranean crossing longitude). For 29 birds, it was possible to directly extract the longitude at crossing latitude 35 N°. For the rest of the cases, the birds had not reached latitude 35 N° before the latitude was obscured by the equinox, we calculated the mean longitude of 10 days from the onset of fall equinox as a measure of the Mediterranean crossing. This measurement correlated highly with the winter longitude (r = 0.78, p = 2.8 × 10−16). To control for the birds relative breeding site longitude, we extracted the departure direction (1°–360°) relative from the tagging site to the location where the birds crossed the Mediterranean (departure direction). The departure data was of circular type (measured in 360°), however the variance did not span more than 180° degrees (range 151°–224°). Therefore, we proceeded with analyses using linear statistics. Geographic distances and departure direction were calculated using R package “geosphere” (version 1.5-10). Complete set of positions of each individual bird with equinoxes excluded is presented in Supplementary Data 1.Laboratory work and molecular data extractionWe extracted DNA from blood samples following the ammonium acetate protocol16. Genotyping for divergent regions on chromosome 1 (InvP-Ch1) and chromosome 5 (InvP-Ch5) was done using a qPCR SNP assay16, which is based on one informative SNP per region (SNP 65 for chromosome 1 and SNP 285 for chromosome 5). Probes and primers were produced by Thermo Fisher Scientific and were designed using the online Custom TaqMan® Assay Design tool (Table S4). We used Bio-Rad CFX96™ Real-time PCR system (Bio-Rad Laboratories, CA, USA) and the universal Fast-two-steps protocol: 95 °C, 15 min—40*(95 °C, 10 s–60 °C, 30 s, plate read. Both regions contain inversion polymorphisms that restrict recombination between subspecies-specific haplotypes and contain nearly all the SNPs separating the two subspecies13. For each region, we scored genotypes as either “Tro” (homozygous for trochilus haplotypes), “Acr” (homozygous for acredula haplotypes) or “Het” (heterozygous). The method that we used to assess the presence of MARB-a is based on a qPCR assay that quantifies the copy number of a novel TE (previously known as AFLP-WW212) that has expanded in acredula. The quantification of repeats by this method has been shown to be highly repeatable (R2 = 0.88) when comparing estimates obtained from DNA in blood and feathers15. We used the forward (5′-CCTTGCATACTTCTATTTCTCCC-3′) and reverse (5′-CATAGGACAGACATTGTTGAGG-3′) primers developed by Caballero-López et al.15 to amplify the TE motif. For reference of a single copy region we used the primers SFRS3F and SFRS3R27. We diluted DNA to 1 ng/μl−1 and used a Bio-Rad CFX96™ Real-time PCR system (Bio-Rad Laboratories, CA, USA) with SYBR-green-based detection. Total reaction volume was 25 μl of which 4 μl of DNA, 12.5 μl of SuperMix, 0.1 μl ROX, 1 μl of primer (forward and reverse), and 6.4 μl of double distilled H2O. We ran quantifications of the single copy gene and the TE variant found on MARB-a on separate plates with the following settings: 50 °C for 2 min as initial incubation, 95 °C for 2 min X 43 (94 °C for 30 s [55.3 °C SFRS3 and 55.5 °C for TE, 30 s] and 72 °C for 45 s). Each sample was run in duplicate and together with a two-fold serial standard dilution (2.5–7.8 × 10−2 ng). Allopatric trochilus have 0–6 copies whereas allopatric acredula have 8–45 copies15; a bimodal distribution was also confirmed in this new data set (Fig. S2). Accordingly, for the present analyses, we split the data in two groups: birds with ≤6 TE copies and birds with >7, translating into absence or presence of MARB-a, with the former assumed to be homozygous for the absence of MARB-a and the latter heterozygous or homozygous for the presence of MARB-a. Data from two investigated willow warbler families suggest a Mendelian inheritance pattern and provide support for our interpretation of how TE copy numbers reflect the three genotypes (Table S5). Moreover, the TE copy numbers within the hybrid swarm have a distribution similar to a combination of allopatric trochilus and acredula, further supporting that the copies are inherited as intact blocks (haplotypes). However, a precise distinction between heterozygotes and homozygotes on MARB-a is still not possible15.Statistical analysisWe used linear models with departure direction, winter longitude, migration distance and departure timing as response variables and the three genetic markers: MARB-a (a factor with two levels), InvP-Ch1 (a factor with three levels) and InvP-Ch5 (a factor with three levels) as explanatory variables. Models were constructed with R base package “stats”. We reported Type II ANOVA for models with more than one explanatory variable and no interactions and type III ANOVA results for models with interaction term by using R package “Car” (version 3.0-12)28. We initially constructed mixed effect models with timing of departure and tagging year as random factors however, this delivered singular fits due to insufficient sample sizes across categories. Normality of residuals was checked with a Shapiro–Wilk test. For carrying out circular statistics on autumn migration direction we used the R package “circular” (version 0.4-93). Watson’s U2 pairwise comparisons of different groups delivered the same results as linear models (Table S2 and Fig. S5). Circular means were identical to conventional linear means in our data set, which we take as another evidence that linear models are appropriate for the analysis of our data (Table S3 and Fig. S5). Maps in Figs. 1 and 2b and S1, S3 and S4 were created with R package “ggplot2” (version 3.3.6) using continent contours from Natural Earth, naturalearthdata.com/. Heat gradient over the maps in Fig. 1a–d were created with R package “gstat” (version 2.0-8) and the inverse distance weighting power of 3.0. Circular plots were created with ORIANA (version 4.02). All analyses were carried out with R version 4.1.1 (R Core Team 2021).Reporting summaryFurther information on research design is available in the Nature Portfolio Reporting Summary linked to this article. More

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    Publisher Correction: Seasonal peak photosynthesis is hindered by late canopy development in northern ecosystems

    Institute of Carbon Neutrality, Sino-French Institute for Earth System Science, College of Urban and Environmental Sciences, Peking University, Beijing, ChinaQian Zhao, Yao Zhang & Shilong PiaoSchool of Urban Planning and Design, Shenzhen Graduate School, Peking University, Shenzhen, ChinaZaichun Zhu & Hui ZengKey Laboratory of Earth Surface System and Human—Earth Relations, Ministry of Natural Resources of China, Shenzhen Graduate School, Peking University, Shenzhen, ChinaZaichun Zhu & Hui ZengDepartment of Earth and Environment, Boston University, Boston, MA, USARanga B. MyneniCSIC, Global Ecology Unit CREAF-CSIC-UAB, Barcelona, Catalonia, SpainJosep PeñuelasCREAF, Barcelona, Catalonia, SpainJosep PeñuelasState Key Laboratory of Tibetan Plateau Earth System, Resources and Environment (TPESRE), Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing, ChinaShilong Piao More